Changes in circadian rhythms during puberty in Rattus norvegicus: Developmental time course and gonadal dependency

Abstract

During puberty, humans develop a later chronotype, exhibiting a phase-delayed daily rest/activity rhythm. The purpose of this study was to determine: 1) whether similar changes in chronotype occur during puberty in a laboratory rodent species, 2) whether these changes are due to pubertal hormones affecting the circadian timekeeping system. We tracked the phasing and distribution of wheel-running activity rhythms during post-weaning development in rats that were gonadectomized before puberty or left intact. We found that intact peripubertal rats had activity rhythms that were phase-delayed relative to adults. Young rats also exhibited a bimodal nocturnal activity distribution. As puberty progressed, bimodality diminished and late-night activity phase-advanced until it consolidated with early-night activity. By late puberty, intact rats showed a strong, unimodal rhythm that peaked at the beginning of the night. These pubertal changes in circadian phase were more pronounced in males than females. Increases in gonadal hormones during puberty partially accounted for these changes, as rats that were gonadectomized before puberty demonstrated smaller phase changes than intact rats and maintained ultradian rhythms into adulthood. We investigated the role of photic entrainment by comparing circadian development under constant and entrained conditions. We found that the period(τ) of free-running rhythms developed sex differences during puberty. These changes in τ did not account for pubertal changes in entrained circadian phase, as the consolidation of activity at the beginning of the subjective night persisted under constant conditions in both sexes. We conclude that the circadian system continues to develop in a hormone-sensitive manner during puberty.

Suprachiasmatic nucleus as the site of androgen action on circadian rhythms

“…Rhythms and sleep change during development and with aging, and there is a strong correspondence between circadian changes and changes in circulating hormone concentration (Roenneberg et al, 2004; Harman et al, 2001). This is supported by a limited number of reports regarding the role of gonadal hormones in organizing circadian rhythms during puberty (Hagenauer et al, 2011a; Hagenauer et al, 2011b). Plasticity of this nature allows organisms to display varied responses to environmental changes, such as those represented in seasonal cycles in temperate zones.…”

“…Among other rhythms, the SCN regulates circadian rhythms in gonadal hormone secretion, and in turn hormones feedback to influence SCN functions (Fernandez-Guasti et al, 2000; Karatsoreos et al, 2007a; Kashon et al, 1996). A role for gonadal hormones in the maturation of circadian rhythmicity has been suggested in rodents and in non-human primates (Hagenauer et al, 2011a; Hagenauer et al, 2011b; Hagenauer and Lee, 2011; Hummer et al, 2012; Melo et al, 2010; Sellix et al, 2013). In humans, there is a correlation between chronotype (morningness or eveningness) and circulating hormone concentrations during aging (Harman et al, 2001; Roenneberg et al, 2004).…”

The Relationship Between Estrogen and the Decline in Delta Power During Adolescence

“…This hypothesis stems from cross-sectional studies in adolescents demonstrating an association between more advanced pubertal stages and a delay in circadian phase preference 11 and is supported by rodent studies linking sex steroids to circadian physiology. 15 Importantly, previous studies of chronotype changes during adolescence suffered not only from the limitations inherent to a cross-sectional study design, but performed pubertal staging according to pubic hair rather breast development, which as previously discussed, does not reflect central puberty or correlate with estrogen exposure.…”

“…11 While this "evening chronotype" has traditionally been attributed to environmental factors (eg, television, computers), studies demonstrating that this phenomenon is preserved under controlled laboratory conditions, 12 is cross-cultural, and predates modern technological advances 13 suggest that it is also likely to be biologically-mediated. Studies reporting an attenuated chronotype shift in gonadectomized animals 14,15 and a sleep timing delay in girls at a younger age than in boys 16 again suggest that sex steroids may be one such mediator. Other studies, however, have found that delayed sleep onset predates physical signs of puberty, 17 arguing against this hypothesis.…”

The neuroendocrine control of the circadian system: Adolescent chronotype

“…The daily rest/activity rhythms of juveniles and early pubertal rodents were characterized by a crepuscular pattern, with the majority of activity occurring near the end of the typical active phase for the species (the end of the night for rats, and the early evening for degus). As puberty progressed, their daily activity began to shift earlier (phase-advance), so that by adulthood most of their activity had consolidated at the beginning of the active phase for the species (Figure 6A , [66-67]). This shift in the timing of daily rest and activity occurred whether we were observing wheel-running activity or general sleep patterns using sleep electrophysiology (degus: [148]; similar data are presented for a small sample size of rats in [76]).…”